When Davis resigned in 1984 he vied for the leadership of the party and won over a slate of three other candidates. In February, 1985 he formed a cabinet of 33 ministers which was the largest cabinet in Ontario's history. Miller quickly called an election which was held on May 2. His party lost 18 seats but still held the most seats with 52. He formed a minority government which lasted less than two months when the Liberals under David Peterson and the New Democrats led by Bob Rae formed an unofficial coalition and defeated the government on a confidence motion on June 26. Initially Miller stayed on as leader of the opposition and vowed to stay on but resigned as leader shortly after.

After retirement from provincial politics he moved back to Muskoka where he became chairman of the District of Muskoka. He died in 2000.

He joined the cabinet of Premier William Davis on February 26, 1974 as Minister of Health.[6] He planned to close a number of small hospitals and consolidate urban services after the 1975 election, but withdrew in the face of cabinet opposition. He suffered a heart attack during this period, perhaps as a result of work-related stress.

Miller became Minister of Natural Resources following a cabinet shuffle on February 3, 1977.[7] On August 16, 1978, he was promoted to Treasurer and Minister of Economics.[8] As Treasurer, he opposed the Davis government's Suncor purchase in 1981 and considered resigning over the issue. After another shuffle on July 6, 1983, he was named Minister of Industry and Trade.[9] In 1983, he gained notoriety for wearing a loud tartan jacket to the 1983 budget ceremony. He was caricatured by some reporters as a symbol of Ontario's rural past, and seemed out of step with generational and demographic changes in the province. Senior party organizerHugh Segal later acknowledged that the jacket probably alienated many new voters.

Davis and his predecessor John Robarts were considered Red Tories and ran relatively progressive administrations that increased public investment and expanded the public sector. Under their watch, the Ontario Tories were often seen, however ironically, to be running left of the Liberals. Miller, on the other hand, was more typical of the party's base of social conservatives from Ontario's rural areas. When Davis officially stepped down on February 8, 1985, Miller became Premier.

Miller's victory created some divisions in the Progressive Conservative Party, and he had difficulty keeping order among senior party staff. He was sometimes criticized for speaking in an overly candid manner to reporters, once claiming that he would prefer to eliminate the minimum wage but could not do so for pragmatic reasons. Miller's appearance also became a political issue, as there were still memories of the tartan-jacket incident of two years earlier.

In February, 1985, Miller announced his first cabinet with a record 33 members including 7 Ministers without portfolio. The size of the cabinet belied Miller's rhetoric of a lean, efficient government. David Peterson called it the "fattest, most bloated Cabinet in the history of this province."[10]

Miller's Progressive Conservatives had a significant lead in the polls of around 55% (compared to the two opposition parties, in the low to mid 20s) when he called an election for May 1985, but his campaign was considered disastrous. He elicited controversy when he refused to agree to a television debate with Liberal leader David Peterson and New Democratic Party leader Bob Rae. This decision is thought to have hurt Miller's standing with the public. His situation was also made more difficult by Davis's decision to extend public funding for CatholicSeparate Schools to grade 13, a decision that had been left to Miller to implement. Although the policy was supported by all parties in the legislature, it was unpopular with some in the Tories' traditional rural Protestant base. Many PC voters were so upset that they simply stayed home on election day because of this issue.

In the election, the Liberals won a narrow plurality of the popular vote. However, at the time rural areas were still overrepresented in the Legislative Assembly, enabling Miller to win reelection. However, the Tories were cut down to a minority government, in which the Tories had only four more seats than the Liberals and were 11 seats short of a majority. The NDP, with 25 seats, held the balance of power.

After several weeks of negotiations with both parties, the NDP signed an agreement with Peterson to support a Liberal minority government. As per this agreement, Rae introduced a Motion of No Confidence in the Miller government, which carried. As a result of the Liberal-NDP accord, Lieutenant-GovernorJohn Black Aird asked Peterson to form a government. Miller formally resigned as Premier on June 26, 1985; ending 42 years of Progressive Conservative rule over Ontario.

Miller resigned as Progressive Conservative leader soon afterward. He was replaced by Larry Grossman in a November 1985 leadership convention. Miller formally resigned as party leader and Leader of the Opposition in early 1986. He played only a minor role in the legislature after this time, and did not seek re-election in 1987. After leaving the legislature, Miller later became chairman of the District of Muskoka.